In 1986, a professional soccer team was again launched in Vancouver, the Vancouver 86ers—so named because of both the year of the team's founding and to commemorate the year Vancouver was founded (1886). Eighty-six people also originally put up $500 each to fund the new team as the West Coast Soccer Society.[3] Led
by player/head coach Bob Lenarduzzi and his assistant Alan Errington, the 86ers were triumphant in their inaugural CSL match, as they defeated Edmonton Brickmen 4–2 in front of 7,646 fans at Swangard Stadium in Burnaby, BC, on June 7, 1987. The 86ers went on to finish second in the Western Division standings that year before bowing out to inaugural league champions Calgary Kickers in the playoff semifinals. The 86ers played in the Canadian Soccer League (CSL) winning 4 straight CSL Championships (1988–1991) and 5 consecutive CSL regular-season first-place finishes (1988–92).

In 1988–1989, the team, coached by Bob Lenarduzzi, set a North American professional sports record by playing 46 consecutive games without a loss.[4] Also in 1988 the Vancouver 86ers and Calgary Kickers played six friendly matches each against the Western Soccer Alliance in the month of May.[5]

In 1990, the Vancouver 86ers captured the North American Club Championship after defeating the Maryland Bays 3–2 in the final played in Burnaby. The game was played between the champions of the Canadian Soccer League and the champions of the American Professional Soccer League (APSL). The 86ers however came up short in the first round of the 1992 Professional Cup North American Club Championship. Facing APSL champions Colorado Foxes over two legs, Vancouver suffered a heartbreaking 3–2 defeat in the first leg in Colorado on August 3, 1992, before the Foxes advanced to the final, as a 2–1 second-leg win at Swangard on August 11, 1992, secured a 5–3 aggregate victory for Colorado. Vancouver played in the CSL from its inception in 1987 until the league folded in 1992, and then moved over to the APSL in 1993 which was later absorbed into the USL hierarchy of leagues in 1997 becoming the A-League, later renamed the USL.

In 2001, the team began to use the old Vancouver Whitecaps moniker (signifying both the 'white caps' of the nearby mountains, and the waves of the Pacific Ocean).
In 2003, the name was again changed, albeit only slightly, to Whitecaps FC, which encompasses the men's, women's, and youth development teams within the organization. At this time, the Whitecaps logo changed slightly in colour (the light teal-green was replaced with a brighter blue) and the word "Vancouver" was dropped from the image.

In 2006, the Whitecaps organization won an unprecedented double-championship, claiming both the United Soccer Leagues First Division championship trophy, defeating the host Rochester Rhinos 3–0 at PAETEC Park, and winning the W-League women's trophy. The men's team also won the Nation's Cup, a new tournament established by their club as a way to feature the Whitecaps playing against international competition. The 2006 Nation's Cup tournament featured the Chinese and Indian U-20 National teams and Championship Welsh club Cardiff City F.C. (the "Bluebirds"). The gradually added the "Vancouver" back into their name, changing it officially to "Vancouver Whitecaps FC".

The following season, the Whitecaps signed a deal to play an exhibition match against the Los Angeles Galaxy, which featured international David Beckham, and promoted Director of Soccer Operations Bob Lenarduzzi to team president.

October 12, 2008, they claimed their second United Soccer Leagues First Division championship with a 2–1 victory over the Puerto Rico Islanders. Charles Gbeke scored twice with his head in the second half to help secure the title. In 2009, they placed 7th in the league and were eliminated in the final by the Montreal Impact on a 6–3 aggregate.[6]

In November 2009 the Whitecaps, along with several other teams, announced their intent to leave the USL First Division to become the co-founders of a new North American Soccer League, which was to begin play in 2010.[7][8] On January 7, 2010 the U.S.S.F. announced that neither the USL nor the NASL would be permitted to have a second division league,[9]
and the USSF would administer a league where the NASL and USL are conferences within the league.[10]

On November 24, 2009 it was announced that Paul Barber, the former Executive Director of Tottenham Hotspur, will become the Chief Executive Operations director of the Caps.[11]

On July 24, 2008, the MLS announced they were seeking to add two expansion franchises for the 2011 season.[13] One day later, the Whitecaps officially announced that they were pursuing one of the two expansion slots. The Whitecaps also announced that local sports icon Steve Nash will join the Whitecaps ownership team.[14]

"There is no doubt the market for professional soccer exists in Vancouver, as we saw last November when nearly 50,000 fans attended the exhibition match between the Los Angeles Galaxy and the Whitecaps, " MLS commissioner Don Garber said.[15]

Vancouver's bid was officially submitted on October 15, 2008, along with bids from 6 other cities.[16] Whitecaps representatives Greg Kerfoot and Jeff Mallett met with MLS officials on November 21, 2008 to go over their bid. Don Garber, who was previously involved in National Football League expansion, described the bid presentation as, "one of the best I've ever seen."[17] Garber and MLS president Mark Abbott were in Vancouver on December 7, 2008 to tour BC Place Stadium and learn about the proposed renovations, which were scheduled to be completed in time for the 2011 MLS season.[18]

Vancouver was officially named an MLS expansion city on March 18, 2009, and joined the league in 2011. They began their inaugural MLS season at Empire Field, a temporary stadium built at the former site of Empire Stadium, and moved into BC Place Stadium[19][20][21][22] when renovations to the stadium were completed.

For some time, the City of Vancouver and the ownership group of the Whitecaps were considering the idea to build the team a soccer-specific stadium called Whitecaps Waterfront Stadium. The new stadium was to be built over the railway tracks east of Waterfront Station on Burrard Inlet.

This 16,000 seat stadium would have replaced Swangard Stadium as the home field for the USL's Vancouver Whitecaps.

There was a fair degree of controversy with regards to this location; a Vancouver council session to debate the issue was extended to four nights to allow public input. Detractors viewed the proposed stadium as an incongruous addition to nearby historic Gastown that would block waterfront access and promote piecemeal development of the area. Proponents of the development felt that the stadium would attract new business to the downtown and Gastown areas, particularly since the soccer team tended to attract a family-oriented audience.

On July 11, 2006, Vancouver City Council voted unanimously to proceed with the stadium project, so long as the Whitecaps could meet certain conditions regarding land use. On January 22, 2007, the Whitecaps filed a new proposal shifting the proposed site for the stadium project to the current location of the SeaBus terminal, a short distance northwest of the previous site.

With the Whitecaps moving up to MLS, the franchise has signed to initially play at Empire Field, and then BC Place Stadium from 2011 to at least 2015. It is hoped that the new facility will be completed by the 2016 MLS season.

The Whitecaps have an independent supporters group known as the Southsiders.[26][27] Founded in 1999, the group is named for their preferred seating area in the south end of Swangard Stadium. The Southsiders, once described as a "rabid supporters group",[28] identify themselves as Canada's oldest supporters association for professional domestic association football.[citation needed]

The group originally called themselves "The Carlsberg Crew," named for the beer company that sponsored Swangard's beer garden. The name was changed to "The Canterbury Chorus" for the subsequent season, as the beer sponsorship had changed between seasons. To avoid changing names every time the sponsor changed, the group chose the name "The Southsiders".[29]